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J. Biol. Chem., Vol. 282, Issue 50, 36593-36602, December 14, 2007

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Expression of Bisecting Type and Lewis^x/Lewis^y Terminated N-Glycans on Human Sperm^*

Poh-Choo Pang, Bérangère Tissot, Erma Z. Drobnis, Peter Sutovsky^¶||, Howard R. Morris^**, Gary F. Clark^¶1, and Anne Dell²

From the Division of Molecular Biosciences, Faculty of Natural Sciences, Imperial College London, London SW7 2AZ, United Kingdom, the Divisions of Reproductive Endocrinology and Infertility and ^¶Reproductive and Perinatal Research, Department of Obstetrics, Gynecology, and Women's Health, School of Medicine, University of Missouri, Columbia, Missouri 65212, the ^||Division of Animal Sciences, University of Missouri, Columbia, Missouri 65202, and ^**M-SCAN Limited, Wokingham, Berks RG41 2TZ, United Kingdom

Human sperm lack major histocompatibility class I molecules, making them susceptible to lysis by natural killer (NK) cells. Major histocompatibility class I negative tumor cells block NK cell lysis by expressing sufficient amounts of bisecting type N-glycans on their surfaces. Therefore, sperm could employ the same strategy to evade NK cell lysis. The total N-glycans derived from sperm were sequenced using ultrasensitive mass spectrometric and conventional approaches. Three major classes of N-glycans were detected, (i) high mannose, (ii) biantennary bisecting type, and (iii) biantennary, triantennary, and tetraantennary oligosaccharides terminated with Lewis^x and Lewis^y sequences. Immunostaining of normal sperm showed that glycoproteins bearing Lewis^y sequences are localized to the acrosome and not the plasma membrane. In contrast, defective sperm showed distinct surface labeling with anti-Lewis^y antibody. The substantial expression of high mannose and complex type N-glycans terminated with Lewis^x and Lewis^y sequences suggests that sperm glycoproteins are highly decorated with ligands for DC-SIGN. Based on previous studies, the addition of such carbohydrate signals should inhibit antigen-specific responses directed against sperm glycoproteins in both the male and female reproductive systems. Thus, the major N-glycans of human sperm are associated with the inhibition of both innate and adaptive immune responses. These results provide more support for the eutherian fetoembryonic defense system hypothesis that links the expression of carbohydrate functional groups to the protection of gametes and the developing human in utero. This study also highlights the usefulness of glycomic profiling for revealing potential physiological functions of glycans expressed in specific cell types.

Received for publication, June 21, 2007 , and in revised form, October 2, 2007.

^* This study was supported by the Wellcome Trust and the Biotechnology and Biological Sciences Research Council (BBSRC) (to A. D. and H. R. M.), a BBSRC professorial fellowship (to A. D.), Imperial College London scholarships and a Malaysian Institute of Strategic and International Studies Perdana Scholarship (to P.-C. P.), National Institutes of Health Grant AI060397-03 (to G. F. C.), the Breeden-Adams Foundation (to G. F. C.), and the Mission Enhancement Program in Reproductive Biology and Medicine (C8783) funded by the state of Missouri (to G. F. C.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Fig. S1 and Table S1.

¹ To whom correspondence may be addressed. Tel.: 573-882-1725; Fax: 757-882-9010; E-mail: clarkgf{at}health.missouri.edu.

² To whom correspondence may be addressed. Tel.: 207-594-5219; Fax: 207-225-0458; E-mail: a.dell{at}imperial.ac.uk.

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